Rates of dinosaur body mass evolution indicate 170 million years of sustained ecological innovation on the avian stem lineage

Abstract

Large-scale adaptive radiations might explain the runaway success of a minority of extant vertebrate clades. This hypothesis predicts, among other things, rapid rates of morphological evolution during the early history of major groups, as lineages invade disparate ecological niches. However, few studies of adaptive radiation have included deep time data, so the links between extant diversity and major extinct radiations are unclear. The intensively studied Mesozoic dinosaur record provides a model system for such investigation, representing an ecologically diverse group that dominated terrestrial ecosystems for 170 million years. Furthermore, with 10,000 species, extant dinosaurs (birds) are the most speciose living tetrapod clade. We assembled composite trees of 614-622 Mesozoic dinosaurs/birds, and a comprehensive body mass dataset using the scaling relationship of limb bone robustness. Maximum-likelihood modelling and the node height test reveal rapid evolutionary rates and a predominance of rapid shifts among size classes in early (Triassic) dinosaurs. This indicates an early burst niche-filling pattern and contrasts with previous studies that favoured gradualistic rates. Subsequently, rates declined in most lineages, which rarely exploited new ecological niches. However, feathered maniraptoran dinosaurs (including Mesozoic birds) sustained rapid evolution from at least the Middle Jurassic, suggesting that these taxa evaded the effects of niche saturation. This indicates that a long evolutionary history of continuing ecological innovation paved the way for a second great radiation of dinosaurs, in birds. We therefore demonstrate links between the predominantly extinct deep time adaptive radiation of non-avian dinosaurs and the phenomenal diversification of birds, via continuing rapid rates of evolution along the phylogenetic stem lineage. This raises the possibility that the uneven distribution of biodiversity results not just from large-scale extrapolation of the process of adaptive radiation in a few extant clades, but also from the maintenance of evolvability on vast time scales across the history of life, in key lineages.

Figure 1. Dinosaur body masses.

(A) Dinosaur body mass through time (the full set of mass estimates is given in Dataset S1). (B) Box-and-whisker plot showing median (dark line), hinges (box range), and ranges (whiskers) of body masses for major dinosaur groups. Outliers (circles) include the iguanodontians Mochlodon vorosi (31 kg), Elrhazosaurus, and Valdosaurus (both 48 kg), the sauropods Europasaurus (1,050 kg) and Magyarosaurus (746 kg), and the flightless avialan Gargantuavis (180 kg).

Figure 2. Node height test for early burst of rates of dinosaur body mass evolution.

(A) Nodal evolutionary rate estimates (standardised independent contrasts [39],[89]) versus node age for data excluding (dashed lowess line) and including (solid lowess line) Maniraptora. (B–C) Box-and-whisker plots detailing results of: (B) robust regression of evolutionary rate on node age: slope (upper plot) and p-value (lower plot); (C) robust regression of evolutionary rate on nodal body mass: slope (upper plot) and p-value (lower plot). In (B–C) dashed lines occur at zero (upper plots) and 0.05 (lower plots: threshold for statistical significance). 1 = Dinosauria; 2 = Ornithischia; 3 = Sauropodomorpha; 4 = Theropoda; and 5 = Maniraptora.

Figure 3. Dinosaur phylogeny showing nodes with exceptional rates of body size evolution.

Exceptional nodes are numbered and indicated by green filled circles with diameter proportional to their down-weighting in robust regression analyses (Appendix S1). Details of these nodes are given in Table 2. The sizes of shapes at tree tips are proportional to log₁₀(mass), and silhouettes are indicative of approximate relative size within some clades. The result from one tree calibrated to stratigraphy by imposing a minimum branch duration of 1 Ma is shown; other trees and calibration methods retrieve similar results. Silhouettes used were either previously available under Public Domain or with permission from the artists. Non-avialan dinosaur silhouettes used with thanks to the artist, Scott Hartman. Avialan silhouettes are modified from work by Nobumichi Tamura, and /Archaeopteryx/ from Mike Keesey.